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Abstract

Current trends in patient care include the desire for minimizing invasiveness of procedures
and interventions. This aim is reflected in the increasing utilization of sentinel
lymph node biopsy, which results in a lower level of morbidity in breast cancer staging,
in comparison to extensive conventional axillary dissection. Optimized lymphoscintigraphy
with triangulated body marking is a clinical option that can further reduce morbidity,
more than when a hand held gamma probe alone is utilized. Unfortunately it is often
either overlooked or not fully understood, and thus not utilized. This results in
the unnecessary loss of an opportunity to further reduce morbidity.

Optimized lymphoscintigraphy and triangulated body marking provides a detailed 3 dimensional
map of the number and location of the sentinel nodes, available before the first incision
is made. The number, location, relevance based on time/sequence of appearance of the
nodes, all can influence 1) where the incision is made, 2) how extensive the dissection
is, and 3) how many nodes are removed. In addition, complex patterns can arise from
injections. These include prominent lymphatic channels, pseudo-sentinel nodes, echelon
and reverse echelon nodes and even contamination, which are much more difficult to
access with the probe only. With the detailed information provided by optimized lymphoscintigraphy
and triangulated body marking, the surgeon can approach the axilla in a more enlightened
fashion, in contrast to when the less informed probe only method is used. This allows
for better planning, resulting in the best cosmetic effect and less trauma to the
tissues, further reducing morbidity while maintaining adequate sampling of the sentinel
node(s).

Introduction

The only goal of sentinel lymph node biopsy (SLNB) is to prevent/reduce morbidity
associated with axillary lymph node dissection (ALND) while maintaining or enhancing
sensitivity for detecting nodal disease. It has been extensively demonstrated that
SLNB is associated with lower morbidity than ALND [1-24]. Lymphoscintigraphy potentially offers further reductions in morbidity, as compared
to a probe-only methodology.

Some surgeons do not utilize lymphoscintigraphy at the time of SLNB and controversies
continue [11,25-36]. One factor that adds confusion to understanding the value of lymphoscintigraphy
is that when it is performed, there is often wide variation in techniques and quality
[37-40], (figure 1). However, when optimized lymphoscintigraphy with triangulated patient body marking
is not performed, an opportunity to further reduce morbidity is missed [38,40,41], [figure 2, table 1, 2, 3]. Below is a discussion of the advantages of lymphoscintigraphy, in which we seek
to clarify misconceptions about its utility, discuss optimal techniques, provide an
updated review of literature available on the added benefits of lymphoscintigraphy,
and discuss its value in special situations.

Figure 1. (A*) TOP: Labeled as a "typical" lymphoscintigraphy finding in an article disputing
the value of lymphoscintigraphy, the lateral view depicts the poor quality of injection
and imaging technique [37]. The injection site is represented by the solid arrow, the faint, barely visible
SN by the open arrow. (B) BOTTOM: Right lateral view of typical/average result from
optimized injection and imaging protocol showing injection sites (solid arrow) and
bright sentinel node (open arrow) as well as lymphatic channel leading to sentinel
node [38]. In many cases, even much brighter nodes than depicted in B are found. *Reprinted from Am J Surg. 177, Burak WE Jr, Routine preoperative lymphoscintigraphy
is not necessary prior to sentinel node biopsy for breast cancer, 445–449., 1999,
with permission from Elsevier Ltd.; Excerpta Medica Inc . [37].

Figure 2. Schematic of triangulated patient body marking technique. Different colored permanent
markers are used to place reference points on the patient's body corresponding to
the location of a sentinel node along a particular projection. With this form of triangulation,
the location of the sentinel nodes can be defined in 3 dimensions along appropriate
triangulation lines. The arm is maintained in the surgical position (90°) to eliminate
shifting of skin markings*. The rotation of the torso referenced to the floor must
be kept constant during both imaging and surgery for the relationships to remain valid,
or compensated for by equally shifted projections if rotation is desired during surgery
[40]. *Adapted, revised and used with permission from Radiographics . 2004;24:121–145. Krynyckyi BR, et al. RSNA Publications, Oak Brook, IL. [ref. 38].

Table 1. Comparisons of average chronic pain and numbness/paresthesia morbidity between LS
groups (+) performing lymphoscintigraphy and non LS groups (-) not performing lymphoscintigraphy
in patients undergoing SLNB using radiotracer or using only dye. In general, studies
using lymphoscintigraphy have much lower levels of chronic sensory morbidity. Data
from original reference by Kim SC et al. [41].

Table 2. Updated comparisons of average chronic pain and numbness/paresthesia morbidity between
LS groups (+) performing lymphoscintigraphy and non LS groups (-) not performing lymphoscintigraphy
in patients undergoing SLNB using radiotracer or using only dye. In general, studies
using lymphoscintigraphy continue to have much lower levels of chronic sensory morbidity.
Updated data by incorporation of four new references [21,22,23,24].

Advantages of lymphoscintigraphy

Wide field of view

Optimized lymphoscintigraphy provides detailed, comprehensive information on sentinel
node (SN) location and on drainage routes. It has the advantage of simultaneously
sampling the entire chest for minutes at a time, in contrast to the probe, which samples
only one particular point for a short time [38,42-45]. Given this enhanced global sensitivity, the camera is superior in the initial survey.
In addition, the images allow identification of internal mammary and other extra axillary
nodes [46-48] and rare cases of drainage to the contralateral axilla [49-53]. When SLNB is performed in patients with previous breast implant augmentation (where
complex patterns of activity can arise), or in cases of previous SLNB, the images
can prove invaluable [54-57].

Unique drainage patterns visualized

In melanoma, lymphoscintigraphy is accepted because globally unique drainage patterns
exist. Information from the images potentially improves staging by mapping out drainage
basins [58,59]. This advantage can be applied to the axilla in breast cancer patients, but on a
smaller, finer scale. Even limited to the region of the axilla, lymphoscintigraphy
can provide similar, detailed information, as the axilla contains multiple nodes at
various levels.

Triangulated body markings improve precision

Utilizing lymphoscintigraphy, an accurate initial incision location and dissection
route can be chosen in advance. When the patient's skin is marked with triangulation
points during lymphoscintigraphy, the surgeon can place the incision optimally. The
triangulation marks result in a 3-Dimensional pattern, which can help to direct the
surgeon to the location of the nodes, especially in obese patients or those with faint
SNs [38,40,43], (Figure 2). Consequently, the initial incision location and dissection route can be better
planned for the best cosmetics and least tissue disruption. This is in contrast to
an approach using only the probe without surface markings, which might be equivocal
during the initial survey in some patients.

Invasiveness can be further minimized

Clinical practice reveals a clear trend for minimally invasive techniques and breast
conservation during both initial diagnosis, staging and subsequent surgical treatment
[60-66]. The additional localizing information provided by optimized lymphoscintigraphy will
allow for fine tuning of the axillary surgical approach in many patients, further
optimizing morbidity reduction.

Additional views (standing/sitting) are possible

The standing/sitting views that are possible with lymphoscintigraphy further improve
accuracy. These views reveal adjacent nodes hidden by the injection site scatter.
They also resolve "clumping" of sentinel nodes that can occur in the axilla in the
supine patient while also eliminating negative "end on effects" of lymphatic channels
which will be discussed below [38,43,67-69]. This is important in delineating the true number of radioactive nodes, and also
informs the surgeons of what to expect, and how many nodes to potentially remove [70,71]. The standing position obviously can not be performed with the probe at the initial
survey before incision once anesthesia is administered.

Optimizing techniques

Injection technique and Hot nodes

Injection technique is an important factor contributing to the ease of finding the
SN and the success of SLNB. Areolar-cutaneous junction injections and similar injections
under the nipple increase SN activity, making the SN easier to find with the probe
while generating optimal images [38,43,72]. These injections are very efficient in delivering activity to the SN, more so than
perilesional or even intra/sub-dermal injections [72]. This is particularly important in the obese patient, where fat attenuates radioactivity
and also increases distances between the SN and probe. In the setting of 15 cm of
fat, less than 20% of the signal is left after attenuation. Increased distance further
weakens the signal by 1/d2 (d = distance from probe to node) and directionality suffers [42,73]. Gamma camera sensitivity, conversely, does not appreciably change over distance
[73].

Augmenting activity in the SN also facilitates next day surgery protocols [11,38,43,72,74-76]. Eighteen hours after injection, the 99mTc radiotracer has decayed to where only 12.5% of the original activity remains in
the SN [73]. Performing injections and obtaining images using protocols that augment SN activity
on the day before surgery, will alleviate surgical scheduling issues/delays. It can
also save operating room time, by avoiding potential delays caused by starting the
technique in the morning. These advantages will result in a cost savings [74-76].

Role of blue dye

When fully optimized lymphoscintigraphy with hybrid combination radiotracer injections
is performed [38,43,72,77], it is no longer necessary to utilize blue dye as a primary method of finding the
SN. In this setting, blue dye serves primarily as a backup (in the rare cases when
a radioactive node is not detected) or as a secondary method to find the SN. Dye also
serves as a potential visual guide when probe directionality is occasionally poor.
Overall, dye provides less benefit than radiotracer as noted in several studies [78-80].

An exclusively blue dye technique can be viewed as not fully fulfilling the primary
goal of morbidity reduction that SLNB promises. It necessitates more extensive dissection,
as the lymphatic ducts leading to nodes are exposed until the SNs are found. In comparison,
probe guided SN extraction can variably detect the SN directly through tissues, and
further guidance is provided by lymphoscintigraphy images and skin markings [81-83].

Some early studies have shown 19.7% to 32.2% of SNs detected by dye alone in patients
where radiotracer was also used [84,85]. However, these studies utilized inefficient perilesional injection techniques and
no imaging methods (probe guided only).

In contrast, King et al. used dermal injections of radiocolloid employing lymphoscintigraphy
and perilesional injections of dye. It was demonstrated that in 1719 procedures, only
1.9% of all the SNs were blue-only, and did not contain radioactivity detected by
probe [86]. In a subgroup of procedures where smaller volumes of dye were used (0.1 ml–1.0 ml),
only 1.3% of SNs were identified by blue dye alone [86]. The rate of blue only SNs positive for disease was higher however, at 10.5%. This
may reflect the lack of simultaneous perilesional and areolar radiotracer injections
as part of a hybrid injection technique as suggested by our group, as only 85.8% of
studies demonstrated nodes on the images [72,86]. With experience in using radiotracer, use of dye becomes less relevant as was demonstrated
in a study of 500 patients by Derossis et al. where a SN identified only with dye
and containing disease was seen in only 2% of cases [87].

In a recent study, Degnim et al. [88] report on 418 cases in which radiotracer and dye were concurrently administered for
SLNB. In 380 of these, SNs were identified on the lymphoscintigraphy images, and were
recovered with the probe and/or by visual guidance from the blue dye. In only 3 of
these 380 cases (0.79%) was disease that altered patient staging found in a node that
contained blue dye but did not contain radioactivity [88]. In other words, had dye not been used, disease that changed staging would have been
missed in 0.79% of total cases where SNs were identified on lymphoscintigraphy [88]. It is possible that technical issues, i.e., suboptimal SN intensity resulting from
using mainly perilesional and dermal over the tumor injections, played a role in these
findings. SNs were demonstrated on lymphoscintigraphy images in only 90.9% (380/418)
of total cases administered radiotracer and dye. This is generally below the expected
SN lymphoscintigraphy visualization rate obtained with current optimal areolar radiotracer
injection methods and camera imaging protocols. Optimal delivery of radiotracer to
SNs is an important issue, because the SNs involved with tumor may have limited numbers
of macrophages, which can make the nodes appear faint if the delivery of radiotracer
is suboptimal [38,40,72,74]. Higher efficiency areolar injections will generally increase activity in SNs proportionally.
This will reduce occurrences of faint, disease containing nodes that are below the
threshold of detection by the probe and camera, resulting in these nodes being missed
by these methods, but visualized with dye. Thus, it can be postulated that even lower
rates of blue node only disease would have been found if more efficient methods of
radiotracer injection and imaging were employed in this study. This needs to be formally
investigated.

In a study utilizing a variant of our previously reported hybrid combination injections
of dermal and perilesional radiocolloid [77,89], without using any blue dye injections at all, Freezer et al. demonstrated a total
2% false negative rate for SLNB in cases that received ALND who had dynamic lymphoscintigraphy
with triangulated skin markings [90].

Lastly, King et al. [86] also reported on 143 patients undergoing prophylactic mastectomy and SN biopsy. Of
these patients, 9.1% had occult carcinoma identified, and the SN was positive in only
1.4% (2/143). In these particular low risk patients, the estimated probability of
a blue-only SN not containing any radioactivity that would alter patient stage is
a very small fraction of that 1.4%. Thus the use of dye in any capacity in this limited
context that may lead to additional dissection can certainly be questioned.

Allergic/anaphylactic reactions, tattooing of skin with surface injections and localized
tissue inflammation have been reported as complications to dye [86,90,91].

Examination of arguments against the use of lymphoscintigraphy

Several articles on lymphoscintigraphy question the value of imaging, and report no
significant difference in the number of SNs found with and without images [37,92,93]. However, it is important to note that both injection and imaging techniques were
key factors in these reports. Universally, less effective perilesional injections
and non-optimized imaging techniques were utilized.

McMasters et al. reported that only 56% of patients who had lymphoscintigraphy performed
showed axillary nodes. In addition, 36.2% showed no drainage to any basin at all on
the lymphoscintigraphy images [92]. However, these results were certainly influenced by technique. The study was multi-center,
and was performed in 1997–1999, with only delayed views after 45–60 minutes (no dynamic
images). Only perilesional injections were utilized, not the currently preferred areolar
or dermal injections [92]. Considering the variation in quality of the lymphoscintigraphy procedures performed
at the different centers, this study cannot accurately reflect what is possible with
optimized techniques of imaging, injection and triangulated patient body marking [38,43-45,72,94-96]. In fact, with current techniques, rates of visualization on lymphoscintigraphy are
97%–100% [11,94-96].

In a study by Burak et al. the authors conclude that routine preoperative lymphoscintigraphy
is not necessary. However, in this study, image quality was severely compromised,
and sentinel nodes were noted on the images in only 70.8% of patients. In addition
to poor image quality, this study was based on a relatively small sample size: 24
patients, (figure 1) [37]. Furthermore, imaging was performed utilizing a lead shielding technique, and the
results were very poor when the tumors were in the upper outer quadrant.

In a larger, Department of Defense study by DuPont et al. involving 516 patients who
had imaging in 1997–1999, only 65% of patients demonstrated axillary nodes during
lymphoscintigraphy [93]. However, here technical aspects again affected the findings. In this study, a suboptimally
narrow energy window of 10% was used as opposed to an upwardly offset 16%–18% energy
window which is recommended [38,43,73,96]. Again, only perilesional injections were used, and shielding of the injection site
was also employed. The reported methods of Burak et al. and DuPont et al. also suggest
that it is likely that suboptimal collimators were used, along with un-optimized image
acquisition energy settings [38,43,73,96,97]. These technical shortcomings can be redressed by using high quality cast (non-foil)
collimators and optimal camera energy settings, which completely obviate the need
for lead shielding. Lead shielding complicates lymphoscintigraphy imaging greatly,
and can lead to artifacts, missed sentinel nodes and false nodes [38,96,97].

Clearly, these studies were influenced by significant technical limitations, as evidenced
by the described methods and/or poor quality sample images presented (figure 1). Furthermore, suboptimal injection technique also contributed to the findings, in
that the more efficient injection methods (dermal or areolar) were not utilized. Unfortunately,
these articles [37,92,93] still continue to be cited as proof of the lack of usefulness of lymphoscintigraphy
[98,99]. Most importantly, none of them address the issues of potential morbidity reduction
that the newer imaging techniques provide, focusing instead mainly on the SN detection
rate or false negative rate [37,40,41,92,93].

A new look at the literature on morbidity reduction with lymphoscintigraphy

Unfortunately, to date, no landmark study has been performed that directly compares
the additional reduction in morbidity achieved by properly performed lymphoscintigraphy,
(with optimal injection technique and triangulated patient body markings) vs. use
of the probe alone or dye alone. In the absence of such a study, we recently performed
a focused review of the literature, which indirectly sheds light on this question
[41].

Kim SC et al. [41] reviewed 20 articles addressing the differences in morbidity between SLNB and ALND.
Of these 20 articles, the authors identified 10 articles in which lymphoscintigraphy
was used that were suitable for comparison to the 3 articles identified in which lymphoscintigraphy
was not utilized [41].

The percentage of patients experiencing chronic sensory morbidity after SLNB in Kim's
analysis of these articles are depicted in Table 1. It is very important to note that multiple confounding issues may exist when comparing
morbidity findings among different studies. However, at the very least, a clear trend
seems to be present in Kim's analysis, which reveals that nearly twice the chronic
sensory morbidity was reported from SLNB in the articles not utilizing lymphoscintigraphy
but using only the probe or using only dye, vs. those articles using both lymphoscintigraphy
and the probe [41], [Table 1].

Subsequent to Kim's analysis, Purushotham AD et al. [21] reported on the results of a randomized controlled clinical trial conducted in patients
with primary breast cancer, which sought to compare morbidity associated with SLNB
and ALND. Three hospitals participated in this study, in which patients were randomly
assigned to ALND or SLNB. The SLNB procedure included radiotracer and blue dye. Personal
communication with authors of this study revealed the following: in all 3 hospitals,
in the SLNB arm, in the majority of cases, lymphoscintigraphy was not performed and/or
if performed, was done suboptimally. In one hospital, the use of lymphoscintigraphy
was abandoned half way through the study due to a perceived lack of usefulness. In
another hospital lymphoscintigraphy was not used in the vast majority of cases. In
the third hospital, lymphoscintigraphy was used only because it was required by the
clinical protocols of that hospital (a surgical teaching hospital), however, the imaging
specialist's reports concerning the results of lymphoscintigraphy were not communicated
to the surgeons prior to surgery [21]. In addition, at this hospital, SNs were not marked on the patient's bodies, thus
the opportunity to utilize triangulated body marking, which provides surgeons with
a reference for SN location in the body, was missed [21,38,40,44,45,57].

Updated evaluation of the literature

In the vast majority of the cases in the study by Purushotham AD et al., lymphoscintigraphy
was either used suboptimally or not at all [21]. Therefore, for the purposes of comparative analysis to other studies, it can be
considered to be a non-lymphoscintigraphy study. Purushotham's study (non lymphoscintigraphy)
[21], along with three new studies in which lymphoscintigraphy was used [22-24], was subjected to the inclusion/exclusion criteria utilized by Kim et al. [41] in their previous analysis, and the data from these four new studies was integrated
into Kim's previous data. A new analysis of the updated dataset was performed. The
results are represented in Table 2.

This table shows that the incorporation of the new data confirms and strengthens the
trend suggested in Kim's previous analysis [41]. The updated analysis demonstrates over twice the chronic sensory morbidity among
the studies not using lymphoscintigraphy but using probe-only or dye-only (P < 0.0001.)

It is interesting to note that, in general, the authors of the articles with the highest
long term sensory morbidity who did not use lymphoscintigraphy, or abandoned/discounted
(as shown in Table 1 and 2 above) have also published the vast majority of articles questioning its overall
value [3,6,18,21,37,92,98-105]. This may be due to their past experiences with lymphoscintigraphy, which have convinced
them of its lack of utility. However, it is quite possible that the lymphoscintigraphy
protocols that were utilized in the past by these authors may have been affected by
serious technical issues (such as were described above), resulting in suboptimal images
of limited utility. Furthermore, it is likely that triangulated body marking was not
used to guide and reduce dissection and subsequent morbidity. Based on our extensive
clinical experience, we are aware that there is clearly great variation in the quality
and methods of lymphoscintigraphy being practiced [37-40].

Intraoperative injections vs. lymphoscintigraphy

Layeeque et al. propose injecting the 99mTc sulfur colloid intra-operatively to eliminate the pain of injection, suggesting
that vasovagal episodes and pain occur 10%–20% of the time with preoperative radiotracer
injections [106]. In our experience pain can be well controlled by a combination of topical anesthetic
applied to the skin and the simultaneous addition of anesthetic to the 99mTc sulfur colloid syringe [38,43,72,77].

Layeeque et al. [106] also suggests that with intraoperative areolar radiotracer injections, lymphoscintigraphy
can be avoided as a result of the improved efficiency of delivering radiocolloid to
the SN provided by surface injections and by the rapid flow of tracer to the SN from
the injection site, which can reach the sentinel node before the injection is completed
[38,43,72,107]. Hotter nodes are easier to find with the probe, and there have been minor advances
in probe design, promising slightly better directionality in future models [108]. However, these superficial injection techniques are accompanied by unique features
that make the images obtained during lymphoscintigraphy, including delayed views,
all the more important.

Performed during surgery or in the nuclear medicine department, areolar injections
will produce very prominent lymphatic channels. These can complicate the removal of
nodes due to the extreme activity that can be present in them. Immediately after areolar
injection, a very dynamic process occurs. Prominent channels appear, often multiple,
that often course a tortuous path [38,43-45,69,72,96,107,109-111]. Nodes can blend in with channels for over 30–120 minutes after injection. Additionally,
channels can track superficially above the axillary SN before coursing internally
and inferiorly to the SN, in an inverted J pattern [38,43,72]. At inflections in the channels, activity can appear as foci, since the observer
is looking at times down/through the length of the channel as opposed to perpendicular
to it (the end on effect) [38,43,69,77,107]. These end on effects are also noted in all regions of the breast. Dilations/ectasias,
which appear immediately after injection, pose an additional problem for the surgeon
as they represent pseudo sentinel nodes and can appear as distinct foci. These are
much more common with the areolar injection techniques compared to perilesional injections,
as much more activity over a shorter time period is concentrated in the lymphatic
channels [38,43,72,107].

During the initial 30–120 minutes after intraoperative injection, the surgeon is faced
with a constantly changing pattern of radioactivity. Pursuing what appear to be foci
that in fact represent end on effects or pseudo sentinel nodes and not real nodes,
can result in unnecessary dissection when using only the probe [38,43,69,72,77,107,111]. Because these complex patterns arise immediately after injection and the changes
continue over time, the information the camera provides in the form of dynamic images,
multi-angle views and delayed views, is valuable in resolving the true nature of the
patterns, a process in which the probe is severely disadvantaged. In fact, intraoperative
injections could actually prolong surgery and increase dissection/morbidity in some
patients, as a result of the complex post injection dynamic patterns described above
[38,43,45,55,68,69,72,74,96,106,107,110-112]. If internal mammary sentinel nodes are deemed important to visualize, then the use
of concurrent perilesional injections as part of a hybrid injection protocol of areolar
and perilesional injections is necessary, as areolar injections do not delineate internal
mammary nodes to any extent [38,72,113-115]. Perilesional injections require much more time to visualize the sentinel nodes than
areolar injections.

Value of lymphoscintigraphy in special situations

There are a number of special situations in which information provided by lymphoscintigraphy
is very valuable. These include situations of non-visualization of nodes, training,
contamination, free pertechnetate, pregnancy and the elderly.

Even with the best areolar injection techniques, there are rare occasions when the
nodes are not seen or only appear after an extended time period [72]. This can occur in older patients, obese patients or those with prior lumpectomies
[43,72,77,110,116]. Knowing that the activity is weak or absent, an additional injection can be performed
employing a higher dose and/or volume of radiotracer [40,72,112].

A final quality control check of the radiotracer occurs with imaging. This will readily
show patterns of free pertechnetate, as well as surface contamination, which are more
difficult to detect with the probe [38,40,77].

In situations where surgeons are in the initial steps of learning SLNB, a lack of
lymphoscintigraphy images and triangulation reference points can be detrimental to
the patient. SLNB is being performed with increasing frequency, fueled by demand from
patients and prevailing trends. In the past SLNB was performed mostly by experienced
investigators with a strong commitment to the technique. However, with rising demand,
a greater number of less experienced mainstream surgeons are adopting SLNB (in some
cases reluctantly), and performing the procedure. Here the lymphoscintigraphy images
serve as a vital training tool, and can support those surgeons who are newly learning
the technique of SLNB. Simulators have been also developed that can assist, along
with the images, in training surgeons [117,118].

In pregnant women and in the elderly, SLNB is safe and accurate [119-121]. Since time spent under anesthesia in these patients should be minimized, knowing
the number and location of sentinel nodes and lymphatic tracts before surgery will
expedite SLNB removal, and accomplish the goal of minimizing anesthesia time.

Limiting the numbers of nodes removed

Using lymphoscintigraphy and triangulation, Kennedy et al. demonstrated that little
benefit in additional sensitivity results from removing more than two sentinel nodes
[122]. Similarly using lymphoscintigraphy, Schrenk et al. suggest that excising more than
three nodes adds little to accuracy [123]. Identifying which node appears first and finding the location of the subsequent,
more distant echelon nodes is even more important with areolar injections than perilesional
injections. This is because areolar injections tend to delineate a greater number
of echelon nodes, as a greater percentage of the injected activity enters more directly
into the lymphatic channels and is available to spill down over to distant echelon
nodes [38,40,43,72,74].

If faced with 6 hot nodes, it is crucial to know which nodes are more important to
excise. Only the first two to four need to be excised if the sequence of appearance
and position along the lymphatic chain is known, especially if both perilesional and
areolar injections of radiotracer first drain to the same primary SN. Therefore, removal
of all remote echelon nodes is probably not warranted in select patients with a very
low probability of nodal disease. Surgeons not utilizing lymphoscintigraphy will be
faced with several dilemmas: 1) not knowing which node was drained to by single or
combination injections, 2) not knowing which node appeared first and second along
the lymphatic channel, 3) not knowing the relative position of all the nodes along
the lymphatic channel and 4) not knowing their relative intensities to each other
before incision. They will need to consider taking all nodes out as the hottest node
is not necessarily the one with disease [124,125]. In contrast, when lymphoscintigraphy has been performed, surgeons can approach the
axilla in a more informed fashion. Furthermore, if only a single node is seen on the
images, and clearly drained to by both perilesional and areolar injections, then extensive
dissection for additional nodes can be avoided to minimize morbidity.

Morbidity reduction is a central goal of SLNB

When nodes are "hot", any reasonably good surgeon can achieve good sensitivity with
varying levels of dissection. The aim is to accomplish this with as little dissection
as possible, and at the same time maintain or improve the sensitivity. Knowing in
advance the total number, location and pattern of SNs and lymphatic channels will
result in a reduction in the total time of surgery, anesthesia, operating room associated
costs, in addition to improved sensitivity. Most importantly a more targeted surgical
approach will result in a reduction in patient morbidity. We observed unique patterns
of drainage that can have an impact on the false negative rate and morbidity [38,43,50,55,69-72,74,77,96,107,113,115]. Based on the vast experience in imaging of multiple authors as well as ourselves
[11,38,40,42-45,47,48,50,55,57,69-72,74,77,96,107,111-115,126-129], the general techniques described here form the basis of a logical algorithm for
patient management.

Summary

SLNB has essentially become the standard of care irrespective of pending prospective
data [132]. Besides the critical questions of false negative rates, equally important emphasis
should be placed on further reducing morbidity by optimization of sentinel node excisional
techniques. In order to accomplish this objective, SLNB methodology should include
1) detailed, optimized lymphoscintigraphy, 2) maneuvers to increase activity within
the SN and 3) triangulated patient body marking. At the present time, in general,
these methods are often either not used (alone or in combination), or if they are
used, are done so in a suboptimal manner. A paradigm shift in departmental methods
is needed to incorporate these valuable techniques, in order to meet the objectives
of minimally invasive surgery, breast conservation and morbidity reduction. While
it is may be true that all women who have SLNB do not benefit directly from lymphoscintigraphy
images, in the patients where the images make a difference and reduce morbidity, a
very meaningful improvement in patient care will have been achieved.

Competing interests

The author(s) declare that they have no competing interests.

Authors' contributions

BRK developed the initial concept and contributed to data analysis, design, revision and
preparation of manuscript.

Kim S, Youssef I, Kim CK, Machac J, Krynyckyi BR: Prominent lymphatic channels simulating sentinel nodes: The utility of standing and
delayed views in delineating the true number and position of nodes and the implications
for further morbidity reduction.